Specialization of primary auditory cortex processing by sound exposure in the “critical period”

Abstract

Environmental acoustic exposure to a complex tone sequence within the critical period in infant rats resulted in the emergence of large-scale, selective changes that radically altered primary auditory cortex (A1) organization. In the sound exposure-revised A1, responses were segregated into two explicit zones representing spectrally and temporally separated lower and higher frequency tone sequence progressions. Cortical neurons between these two A1 zones were poorly driven by sound stimuli. Stimulus sequence-specific (''combination-selective'') responses emerged in the A1 of exposed rats. These selective representational changes induced in the critical period persisted into adulthood. These results show that the temporal order and pace of early, repetitive postnatal auditory inputs strongly affect the emergent and enduring functional organization of A1.A uditory experience plays an important role in the development of the primary auditory cortex (A1) (1-10). Exposure of kittens or rat pups to a modulated tonal stimuli during an early postnatal period resulted in an expansion of the representation of the exposed sound frequency in A1 (2, 7). Synchronous electrical stimulation of a cochlear implant in congenitally deaf cats led to larger cortical regions producing middle-latency evoked responses (11). The formation of an orderly, continuous sound frequency (''tonotopic'') representation and a postnatal sharpening of tonal receptive fields in the rat A1 appeared to require exposure to normally variable auditory inputs during the ''critical period'' (ref. 1, but also see ref. 12 for a difference in cats). However, it remains unclear how the cortical representations of the dynamic aspects of complex sound are specifically shaped by the spectro-temporal patterns of auditory inputs during development. These studies were designed to initiate our attack on this important issue.In this initial study, we exposed rat pups through a critical period epoch extending from postnatal day (P) 9 (before hearing is first functional, at ϷP12) to P30 (when the critical period is drawing to a close) to a tone sequence with two specific spectro-temporal patterns. The frequency representation of A1 was radically revised by the exposure to this complex acoustic stimulus. Cortical neurons developed a preference for the temporal sequences of sound that the infant rat was exposed to. Induced changes endured into adulthood. These results underscore the specific instructive role of early auditory experience in sculpting the specific circuits of the auditory system to selectively and enduringly represent inputs that are present in the criticalperiod acoustic environment. MethodsEarly Exposure of Rat Pups. All of the experimental procedures applied in this study were approved by the University of California San Francisco animal research committee. Litters of nine to twelve 9-day-old female rats (Sprague-Dawley) were placed with their mothers in a calibrated, sound-shielded test chamber from P9 to P30 in the presence of auditory stimulation consi...

Mother’s voice and heartbeat sounds elicit auditory plasticity in the human brain before full gestation

“…Our findings of auditory brain plasticity before full gestation are in keeping with several studies, primarily by Merzenich and colleagues, showing that early auditory experience, either in the form of enrichment or impoverishment, can have a substantial impact on both the structural and functional development of the AC in rat pups (26,27,29,31,57,58). Similarly, an established body of work by Lickliter and colleagues has shown that bobwhite quail chicks receiving auditory stimulation early in embryogenesis demonstrated improved auditory learning and memory when tested postnatally (59)(60)(61).…”

Successive-signal biasing for a learned sound sequence

“…Nakahara et al (19) exposed infant rats to sound sequences within the critical period and showed that this exposure resulted in enduring sequence-specific activation of neurons recorded all across a broad cortical area representing sequence frequencies. Kilgard and Merzenich (5) paired sound sequences with electrical stimulation of the nucleus basalis in adult rats and showed that this pairing resulted in emergent sequencespecific responses that amplified the responses of later stimulus components of conditioned stimulus sequences.…”

Sound sequence discrimination learning motivated by reward requires dopaminergic D2 receptor activation in the rat auditory cortex

“…The auditory response of AC neurons can be modulated by stimulus sequence (McKenna et al 1989;Brosch et al 1999;Brosch and Schreiner 2000), and some AC neurons respond selectively to a particular sequential combination of sounds (Suga et al 1978;Kilgard and Merzenich 2002;Nakahara et al 2004). These studies suggest that sound sequences can be coded by AC neurons.…”

“…The importance of the auditory cortex (AC) in sound sequence discrimination has been suggested by various studies. AC neurons respond selectively to a particular sequence of sounds (Suga et al 1978;Kilgard and Merzenich 2002;Nakahara et al 2004). The auditory response of AC neurons can be either enhanced or inhibited by preceding sounds (McKenna et al 1989;Brosch et al 1999;Brosch and Schreiner 2000).…”